Sexual conflict and evolution in Trinidadian guppies

Recent investigations have highlighted the importance of sexual conflict in the evolution of reproductive isolation. Examination of the Trinidadian guppy (Poecilia reticulata) shows how geographic variation in sexual conflict can mediate the emergence of isolating mechanisms. On the basis of pre-mating behaviour guppy females appear to be winning the battle of the sexes in low risk localities whereas males are apparently ahead in high-predation environments. However, the conclusion that sexual selection (through female choice) is replaced by sexual coercion of females (as a consequence of sneaky mating) in predator rich (and productive) assemblages takes no account of post-copulatory mechanisms. Recent work on sperm competition in guppies suggests coevolution between males and females may also occur in the post-mating, pre-zygotic arena. The potential for the evolution of reproductive isolation at each stage of the mating sequence is assessed.     

Predicting the direction of ornament evolution in Trinidadian guppies (Poecilia reticulata)

Sexual selection is thought to be opposed by natural selection such that ornamental traits express a balance between these two antagonistic influences. Phenotypic variation among populations may indicate local shifts in this balance, or that different stable ‘solutions’ are possible, but testing these alternatives presents a major challenge. In the guppy (Poecilia reticulata), a small freshwater fish with male-limited ornamental coloration, these issues can be addressed by transplanting fish among sites of varying predation pressure, thus effectively manipulating the strength and nature of natural selection. Here, we contrast the evolutionary outcome of two such introductions conducted in the Trinidadian El Cedro and Aripo Rivers. We use sophisticated colour appraisal methods that account for full spectrum colour variation and which incorporate the very latest visual sensitivity data for guppies and their predators. Our data indicate that ornamentation evolved along different trajectories: whereas Aripo males evolved more numerous and/or larger orange, black and iridescent markings, El Cedro males only evolved more extensive and brighter iridescence. Examination of the El Cedro experiment also revealed little or no ornamental evolution at the control site over 29 years, which contrasts markedly with the rapid (approx. 2–3 years) changes reported for introduction populations. Finally, whole colour-pattern analysis suggested that the greatest visual difference between El Cedro introduction and control fish would be perceived by the two most salient viewers: guppies and the putatively dangerous predator Crenicichla alta. We discuss whether and how these evolutionary trajectories may result from founder effects, population-specific mate preferences and/or sensory drive.     

Rapid evolution of escape ability in Trinidadian guppies (Poecilia reticulata)

Predators are widely assumed to create selection that shapes the evolution of prey escape abilities. However, this assumption is difficult to test directly due to the challenge of recording both predation and its evolutionary consequences in the wild. We examined these events by studying natural and experimental populations of Trinidadian guppies, Poecilia reticulata, which occur in distinct high-predation and low-predation environments within streams. Importantly, in the last two decades several populations of guppies have been experimentally introduced from one type of predatory environment into the other, allowing measurements of the consequences of change. We used this system to test two hypotheses: First, that changes in predatory environments create phenotypic selection favoring changes in escape ability of guppies, and second, that this selection can result in rapid evolution. For the first test we compared escape ability of wild caught guppies from high- versus low-predation environments by measuring survival rates during staged encounters with a major predator, the pike cichlid Crenicichla alta. We used guppies from three streams, comparing two within-stream pairs of natural populations and three within-stream pairs of an introduced population versus its natural source population. In every comparison, guppies from the high-predation population showed higher survival. These multiple, parallel divergences in guppy survival phenotype suggest that predatory environment does create selection of escape ability. We tested our second hypothesis by rearing guppies in common garden conditions in the laboratory, then repeating the earlier experiments using the F2 generation. As before, each comparison resulted in higher survival of guppies descended from the high-predation populations, demonstrating that population differences in escape ability have a genetic basis. These results also show that escape ability can evolve very rapidly in nature, that is, within 26-36 generations in the introduced populations. Interestingly, we found rapid evolutionary loss of escape ability in populations introduced into low-predation environments, suggesting that steep fitness trade-offs may influence the evolution of escape traits.     

Parallel and nonparallel behavioural evolution in response to parasitism and predation in Trinidadian guppies

Natural enemies such as predators and parasites are known to shape intraspecific variability of behaviour and personality in natural populations, yet several key questions remain: (i) What is the relative importance of predation vs. parasitism in shaping intraspecific variation of behaviour across generations? (ii) What are the contributions of genetic and plastic effects to this behavioural divergence? (iii) And to what extent are responses to predation and parasitism repeatable across independent evolutionary lineages? We addressed these questions using Trinidadian guppies (Poecilia reticulata) (i) varying in their exposure to dangerous fish predators and Gyrodactylus ectoparasites for (ii) both wild‐caught F0 and laboratory‐reared F2 individuals and coming from (iii) multiple independent evolutionary lineages (i.e. independent drainages). Several key findings emerged. First, a population's history of predation and parasitism influenced behavioural profiles, but to different extent depending on the behaviour considered (activity, shoaling or boldness). Second, we had evidence for some genetic effects of predation regime on behaviour, with differences in activity of F2 laboratory‐reared individuals, but not for parasitism, which had only plastic effects on the boldness of wild‐caught F0 individuals. Third, the two lineages showed a mixture of parallel and nonparallel responses to predation/parasitism, with parallel responses being stronger for predation than for parasitism and for activity and boldness than for shoaling. These findings suggest that different sets of behaviours provide different pay‐offs in alternative predation/parasitism environments and that parasitism has more transient effects in shaping intraspecific variation of behaviour than does predation.     

Disturbance cue communication is shaped by emitter diet and receiver background risk in Trinidadian guppies

In animal communication systems, individuals that detect a cue (i.e., “receivers”) are often influenced by characteristics of the cue emitter. For instance, in many species, receivers avoid chemical cues that are released by emitters experiencing disturbance. These chemical “disturbance cues” appear to benefit receivers by warning them about nearby danger, such as a predator’s approach. While the active ingredients in disturbance cues have been largely unexplored, by-products of metabolized protein are thought to play a role for some species. If so, the content (quality) and volume (quantity) of the emitter’s diet should affect their disturbance cues, thus altering how receivers perceive the cues and respond. Guppies Poecilia reticulata are a species known to discriminate among disturbance cues from different types of donors, but dietary variation has yet to be explored. In this study, we found evidence that diet quality and quantity can affect disturbance cues released by guppy emitters (i.e., experimental “donors”). Receivers discriminated between donor cue treatments, responding more strongly to cues from donors fed a protein-rich bloodworm diet (Experiment 1), as well as an overall larger diet (Experiment 2). We also found that receivers exposed to higher background risk were more sensitive to disturbance cue variation, with the strongest avoidance responses displayed by high-risk receivers toward disturbance cues from donors fed the high-quality diet. Therefore, diet, and perhaps protein specifically, affects either the concentration or composition of disturbance cues released by guppies. Such variation may be important in information signaling in social species like the guppy.     

Diet drives convergent evolution of gut microbiomes in bamboo-eating species

Gut microbiota plays a critical role in host physiology and health. The coevolution between the host and its gut microbes facilitates animal adaptation to its specific ecological niche. Multiple factors such as host diet and phylogeny modulate the structure and function of gut microbiota. However, the relative contribution of each factor in shaping the structure of gut microbiota remains unclear. The giant(Ailuropoda melanoleuca) and red(Ailurus styani) pandas belong to different families of order Carnivora. They have evolved as obligate bamboo-feeders and can be used as a model system for studying the gut microbiome convergent evolution. Here, we compare the structure and function of gut microbiota of the two pandas with their carnivorous relatives using 16S rRNA and metagenome sequencing. We found that both panda species share more similarities in their gut microbiota structure with each other than each species shares with its carnivorous relatives. This indicates that the specialized herbivorous diet rather than host phylogeny is the dominant driver of gut microbiome convergence within Arctoidea.Metagenomic analysis revealed that the symbiotic gut microbiota of both pandas possesses a high level of starch and sucrose metabolism and vitamin B12 biosynthesis. These findings suggest a diet-driven convergence of gut microbiomes and provide new insight into host-microbiota coevolution of these endangered species.     

Adaptive evolution to a high purine and fat diet of carnivorans revealed by gut microbiomes and host genomes

Carnivorous members of the Carnivora reside at the apex of food chains and consume meat‐only diets, rich in purine, fats and protein. Here, we aimed to identify potential adaptive evolutionary signatures compatible with high purine and fat metabolism based on analysis of host genomes and symbiotic gut microbial metagenomes. We found that the gut microbiomes of carnivorous Carnivora (e.g., Felidae, Canidae) clustered in the same clade, and other clades comprised omnivorous and herbivorous Carnivora (e.g., badgers, bears and pandas). The relative proportions of genes encoding enzymes involved in uric acid degradation were higher in the gut microbiomes of meat‐eating carnivorans than plant‐eating species. Adaptive amino acid substitutions in two enzymes, carnitine O‐palmitoyltransferase 1 (CPT1A) and lipase F (LIPF), which play a role in fat digestion, were identified in Felidae‐Candidae species. Carnivorous carnivorans appear to endure diets high in purines and fats via gut microbiomic and genomic adaptations.     

The genetic and environmental basis of adaptive differences in shoaling behaviour among populations of Trinidadian guppies,Poecilia reticulata

The degree of plasticity an individual expresses when moving into a new environment is likely to influence the probability of colonization and potential for subsequent evolution. Yet few empirical examples exist where the ancestral and derived conditions suggest a role for plasticity in adaptive genetic divergence of populations. Here we explore the genetic and plastic components of shoaling behaviour in two pairs of populations of Poecilia reticulata (Trinidadian guppies). We contrast shoaling behaviour of guppies derived from high‐ and low‐predation populations from two separate drainages by measuring the shoaling response of second generation laboratory‐reared individuals in the presence and absence of predator induced alarm pheromones. We find persistent differences in mean shoaling cohesion that suggest a genetic basis; when measured under the same conditions high‐predation guppies form more cohesive shoals than low‐predation guppies. Both high and low‐predation guppies also exhibit plasticity in the response to alarm pheromones, by forming tighter, more cohesive shoals. These patterns suggest a conserved capacity for adaptive behavioural plasticity when moving between variable predation communities that are consistent with models of genetic accommodation.     

Courtship behavior,swimming performance,and microhabitat use of Trinidadian guppies

Synopsis We document differences in the use of microhabitats, male courtship behavior, and swimming performance of populations from headwater and downstream sites in two rivers of the Oropuche drainage in Trinidad. Guppies from headwater sites used microhabitats with higher water velocities, had a higher swimming performance, and were less patchily distributed than guppies from downstream sites. Although males from the headwater and downstream sites had similar display rates, males from headwater sites displayed in microhabitats with higher velocities (riffles) whereas males in downstream sites courted in still pools. Subtle effects of female choice maintain the honesty of male courtship behavior in various microhabitats. In downstream sites, where predators impose a survivorship cost on ornamental males, swimming performance was positively correlated with area of carotenoid ornamentation. In headwater sites, males frequently displayed in fast-flowing water, thus paid a higher metabolic cost of courtship. Interactions between characteristics of the physical habitat and predation pressure not only affect the distribution of guppies, but also have subtle effects on the types of condition-dependent traits favored by females.     

Pace of life,predators and parasites: predator-induced life-history evolution in Trinidadian guppies predicts decrease in parasite tolerance

A common evolutionary response to predation pressure is increased investment in reproduction, ultimately resulting in a fast life history. Theory and comparative studies suggest that short-lived organisms invest less in defence against parasites than those that are longer lived (the pace of life hypothesis). Combining these tenets of evolutionary theory leads to the specific, untested prediction that within species, populations experiencing higher predation pressure invest less in defence against parasites. The Trinidadian guppy, Poecilia reticulata, presents an excellent opportunity to test this prediction: guppy populations in lower courses of rivers experience higher predation pressure, and as a consequence have evolved faster life histories, than those in upper courses. Data from a large-scale field survey showed that fish infected with Gyrodactylus parasites were of a lower body condition (quantified using the scaled mass index) than uninfected fish, but only in lower course populations. Although the evidence we present is correlational, it suggests that upper course guppies sustain lower fitness costs of infection, i.e. are more tolerant, than lower course guppies. The data are therefore consistent with the pace of life hypothesis of parasite defence allocation, and suggest that life-history traits mediate the indirect effect of predators on the parasites of their prey.     

Functional profiling of the gut microbiomes in two different populations of the brown planthopper,Nilaparvata lugens

Previous studies have demonstrated that gut symbionts are involved in the detoxification metabolism of insect hosts, but the relationship between gut symbionts and host detoxification metabolism of the brown planthopper (Nilaparvata lugens, BPH) remains unclear. In the present study, an indoor population (NlIP) and a field population (NlFP) of the BPH were used to characterize the functional profiling of the gut microbiome based on 16S rDNA sequencing. The results show that the NlIP and NlFP strains of N. lugens had different symbiont compositions, and Proteobacteria, Actinobacteria, and Firmicutes were the dominate phyla, accounting for >75% of the total symbiont compositions. Additionally, the NlIP strain had more Pantoea and Stenotrophomonas, while the NlFP strain showed a higher Wolbachia, Actinobacteria, and Herbaspirillum relative abundance. Furthermore, functional content of the metagenome predicted by PICRUSt demonstrated no significant difference in metagenomic function between the NlIP and NlFP strains in the principal component analysis (PCA), and only three types of genes, namely, genes involved with metabolic diseases, poorly characterized genes, and genes involved in circulatory systems, were different between the strains based on KEGG pathway analysis, which also speculated that gut symbionts are not directly involved in the detoxification metabolism for insecticides in the BPH. These results will be helpful for further research into the mechanisms of gut symbionts involved in detoxification metabolism in the BPH.     

Evolutionary implications of large-scale patterns in the ecology of Trinidadian guppies, Poecilia reticulata

Previous investigations of the guppy, Poecilia reticulata , in Trinidad have demonstrated rapid population differentiation at small geographic scales. However, most studies to date have focused on localities in Trinidad's Northern Range where barrier water falls mark sharp discontinuities in the selection regime and limit scope for gene flow. There is little information on the ecology of the guppy in the rest of the island even though its distribution amongst fish communities and habitats has important evolutionary implications. To determine how large-scale distribution patterns might affect the evolutionary potential of the guppy we surveyed 80 sites representative of a broad range of freshwater environments. We found guppies, which occurred in 80% of our samples, to be the most widely distributed freshwater fish in Trinidad. Guppies are common in predator-rich and turbid habitats, precisely those localities where female preferences are likely to be undermined. Moreover, the widespread distribution of this adaptable species, combined with its promiscuous mating system, may promote gene flow across geographical scales that transcend local selection regimes. These factors are likely to impede the evolution of reproductive isolation.     

Social learning of foraging sites and escape routes in wild Trinidadian guppies

We describe two field experiments with wild guppies, Poecilia reticulata, in Trinidad that demonstrated that guppies can acquire foraging and predator escape-response information from conspecifics. In the foraging experiment, subjects were presented with two distinctly marked feeders in their home rivers. One feeder contained a conspecific shoal in a transparent container. Guppies preferred to enter the feeder containing this artificial shoal over the other feeder. In a test phase, the artificial shoal was removed and the feeders replaced at the testing site after a 5-min delay. More guppies entered the feeder that had contained the artificial shoal over the other feeder, a difference that can be explained only by the fish learning the characteristics or location of the feeder during the training phase. We suggest that subjects acquired a foraging patch preference through a propensity to approach feeding conspecifics, a local enhancement process. In the predator escape-response experiment, na?ve ‘observer’ guppies could avoid an approaching trawl net by escaping through either a hole to which ‘demonstrator’ guppies had been trained or through an alternative hole. When the demonstrators were present, the na?ve observers escaped more often and more rapidly by the demonstrated route than the alternative route. When the demonstrators were removed, observers maintained a route preference according to the training of their demonstrators, which suggests that the observers had learned an escape route through following or observing their more knowledgeable conspecifics. Thus, both experiments reveal that guppies can socially learn in the wild. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

Impact of a 7-day homogeneous diet on interpersonal variation in human gut microbiomes and metabolomes

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Caudal eyespots on fish predators influence the inspection behaviour of Trinidadian guppies, Poecilia reticulata

The effect of the false caudal eyespots (ocelli) of fish predators on guppy inspection behaviour was tested by use of predator ( Crenicichla ) models with and without a caudal ocellus. When a false eyespot was present, inspecting guppies spent significantly less time near the tail compared to a control model without a tail eyespot.     

Divergence and convergence in enzyme evolution: parallel evolution of paraoxonases from quorum-quenching lactonases

We discuss the basic features of divergent versus convergent evolution and of the common scenario of parallel evolution. The example of quorum-quenching lactonases is subsequently described. Three different quorum-quenching lactonase families are known, and they belong to three different superfamilies. Their key active-site architectures have converged and are strikingly similar. Curiously, a promiscuous organophosphate hydrolase activity is observed in all three families. We describe the structural and mechanistic features that underline this converged promiscuity and how this promiscuity drove the parallel divergence of organophosphate hydrolases within these lactonase families by either natural or laboratory evolution.     

Divergence and evolution of reproductive barriers among three allopatric populations of Rhagoletis cingulata across eastern North America and Mexico

Geography is often a key factor facilitating population divergence and speciation. In this regard, the geographic distributions of flies in the genus Rhagoletis (Diptera: Tephritidae) in temperate North America have been affected by cycles of Pleistocene glaciation and interglacial periods. Fluctuations in climatic conditions may have had their most dramatic effects on geographically isolating Rhagoletis flies in the central highland region of Mexico. During past periods of allopatry, a degree of post‐zygotic reproductive isolation appears to have evolved between hawthorn‐infesting populations of Rhagoletis pomonella (Walsh) in the central Eje Volcanico Trans Mexicano (EVTM) and those from the Sierra Madre Oriental Mountains (SMO) of Mexico, as well as hawthorn flies from the eastern USA. Here, we investigate the generality of this finding in the genus Rhagoletis by testing for reproductive isolation among populations of Rhagoletis cingulata (Loew) (Diptera: Tephritidae) collected from infested domesticated sweet cherry (Prunus avium L.) in the USA and black cherry [Prunus serotina Ehrh. (both Rosaceae)] from the SMO and EVTM. We report evidence for marked post‐mating reproductive isolation among certain R. cingulata populations. The high levels of reproductive isolation were observed between R. cingulata flies from populations in the USA and SMO differed from the pattern seen for R. pomonella, primarily involving the EVTM. In addition, egg hatch was significantly reduced for crosses between SMO males and EVTM females, but not greatly in the opposite direction. We discuss potential causes for the different patterns of post‐mating reproductive isolation among Rhagoletis flies.     

Artificial introductions, evolutionary change and population differentiation in Trinidadian guppies (Poecilia reticulata; Poeciliidae)

The evolutionary consequences of three artificial introductions of the guppy, Poecilia reticulata , in Trinidad were examined by comparing the allozymic structure (observed heterozygosity ( H _o), and mean number of alleles ( N _a) of each corresponding source (S) and transplant (T) population. In 'Haskins' (H) and EndlerY (E) introduction, 200 guppies (half female) were transferred to guppy-free habitats in 1957 and 1976 respectively. 'Kenny's' (K) introduction in 1981 involved the release of a single pregnant female into an isolated ornamental pond. Analysis of allozyme frequencies at 25 enzyme-coding loci revealed reductions in observed heterozygosity at some loci in all three transplant samples, and a marked decline in the mean number of alleles in Kenny's pond sample. Significant genetic differentiation occurred between (S) and (T) samples at some loci in all introductions, but was most marked in H(T) and K(T). Despite previous studies on rapid evolutionary changes in the life histories and morphology of Endler's transplant guppies, there was little support for any major effects of stochastic forces on allozymic diversity arising from the introduction. Selection arising from changes in predation pressure appeared to be the predominant factor causing the remarkably rapid adaptation of guppies to their new environments. Genetic divergence in some marginal or isolated natural populations was similar to, or greater than, Kenny's pond guppies (Reynolds' genetic distance, R = 0.496), indicating that chance colonization and founder effects may have contributed to the observed geographic patterns of genetic differentiation in Trinidad.     

Ornamental evolution in Trinidadian guppies (Poecilia reticulata): insights from sensory processing‐based analyses of entire colour patterns

The evolution of exaggerated sexual ornamentation is classically thought to proceed as a compromise between opposing vectors of sexual and natural selection. In colour‐based ornamentation, as exhibited by guppies (Poecilia reticulata), heightened trait expression may be beneficial in promoting attractiveness, but costly in terms of predation. Opportunities to reconcile this compromise will exist if there are differences between conspecifics and predators in their sensory systems; in such situations guppies should evolve to exploit the ways in which their ornamentation would appear maximally conspicuous to conspecifics. In the present study, we addressed this hypothesis via a study of geographic variation employing the most sophisticated colour analysis yet attempted for Trinidadian guppies. We made two paired contrasts, one between two Aripo populations that vary in the presence of the potential predator Aequidens pulcher, and another between Quare and Marianne populations that vary in exposure to a predatory prawn, Macrobrachium crenulatum. We predicted that, if ornamentation is constrained by the presence of either predator, then guppy conspicuousness should change most markedly across each of the two paired populations as viewed by that predator. Although disparity analysis of entire colour patterns indicated significant differences in both contrasts, this prediction was most clearly supported for the Marianne/Quare contrast. Marianne fish, which co‐exist with prawns, exhibited larger black spots coupled with less extensive, less bright flank iridescence. The brightness reductions are notable because, as the only potential guppy predator with a dedicated ultraviolet (UV) photoreceptor, prawns may detect passing male guppies via their UV‐bright blues, violets and ‘UV/oranges’. We discuss our findings in light of the additional insights that might be obtained by combining spectral assessments and visual modeling with more traditional methods of colour pattern appraisal. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 734–747.